osseointegration of standard and mini dental implants: a

RESEARCH Open Access

Osseointegration of standard and minidental implants: a histomorphometriccomparisonJagjit S. Dhaliwal1*, Rubens F. Albuquerque Jr2, Monzur Murshed1,3 and Jocelyne S. Feine1

Abstract

Background: Mini dental implants (MDIs) are becoming increasingly popular for rehabilitation of edentulouspatients because of their several advantages. However, there is a lack of evidence on the osseointegration potentialof the MDIs. The objective of the study was to histomorphometrically evaluate and compare bone apposition onthe surface of MDIs and standard implants in a rabbit model.

Methods: Nine New Zealand white rabbits were used for the study to meet statistical criteria for adequate power.Total 18 3M™ESPE™ MDIs and 18 standard implants (Ankylos® Friadent, Dentsply) were inserted randomly into thetibia of rabbits (four implants per rabbit); animals were sacrificed after a 6-week healing period. The specimens wereretrieved en bloc and preserved in 10% formaldehyde solution. Specimens were prepared for embedding in a lightcure acrylic resin (Technovit 9100). The most central sagittal histological sections (30–40 μm thick) were obtainedusing a Leica SP 1600 saw microtome. After staining, the Leica DM2000 microscope was used, the images werecaptured using Olympus DP72 camera and associated software. Bone implant contact (BIC) was measured usingInfinity Analyze software.

Results: All implants were osseointegrated. Histologic measures show mineralized bone matrix in intimate contactwith the implant surface in both groups. The median BIC was 58.5 % (IQR 8.0) in the MDI group and 57.0 % (IQR 5.5)in the control group (P > 0.05; Mann-Whitney test). There were no statistical differences in osseointegration at 6 weeksbetween MDIs and standard implants in rabbit tibias.

Conclusions: Based on these results, it is concluded that osseointegration of MDIs is similar to that ofstandard implants.

Keywords: Bone implant contact, Mini dental implant, Osseointegration

BackgroundThe term “osseointegration” was first introduced toexplain the phenomenon for stable fixation of titaniumto bone by Brånemark et al. in the 1960s [1]. Osseointe-grated implants were introduced, a new era in oralrehabilitation began, and many studies were conducted[2, 3]. A success rate of over 90% has been reported [4, 5].Further, a success rate of 81% in the maxillary bone and91% in the mandible can be accomplished [6]. Dentalimplants have been widely used for the stabilization of

complete dentures and also help to maintain bone, func-tion, esthetics, and phonetics and improve the oral health-related quality of life [7]. The dental implants are availablewith different surfaces and sizes. The size of the dentalimplants usually ranges in the diameter range of 3 mm(narrow diameter) to 7 mm (wide diameter). However,majority of the implants fall in the “standard diameter”range of 3.7 to 4.0 mm [8].Mini dental implants or small size implants are also

being widely used for stabilizing the complete dentures[9], for orthodontic anchorage [10–12], single toothreplacements [13, 14], fixing the surgical guides fordefinitive implant placement [15], and as transitional* Correspondence: [email protected]

1Faculty of Dentistry, McGill University, 2001 McGill College Avenue, Suite500, Montreal, Quebec H3A 1G1, CanadaFull list of author information is available at the end of the article

International Journal ofImplant Dentistry

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Dhaliwal et al. International Journal of Implant Dentistry (2017) 3:15 DOI 10.1186/s40729-017-0079-1

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implants for the support of interim removable prosthesisduring the healing phase of final fixtures [16, 17].The single-piece mini dental implants (MDIs) are

becoming increasingly popular for the purpose of den-ture stabilization. There are many advantages of theMDIs over the regular implants. The surgery is minim-ally invasive as compared with conventional implant sur-gery which helps in decreased morbidity for the patient.Transmucosal placement is possible using a single pilotdrill, and these can often be loaded immediately [18].Gingival healing is typically seen in 2 to 5 days, extendedhealing period with MDIs is usually not necessary [19].The insertion of MDIs needs a minimal disturbance ofthe periosteum, thus osseointegration process is acceler-ated and time needed for MDIs tends to be considerablysmall than that of regular implants due to less injuriousinsertion procedure [9]. The need for sutures or longrecovery periods is eliminated [3]. The patient can walkin to the office in the morning and is out the same daywith a full set of teeth, the patient is allowed to eat thesame day. These can work well for patients who havesignificant bone loss that restrict them from being acandidate for regular dental implants. MDIs are also asolution for patients that cannot have surgery for med-ical reasons. MDIs are also cost effective [20]. Consider-able confusion exists in the literature regarding the bestmethod to monitor the status of a dental implant. Variousmethods have been used to demonstrate the osseointegra-tion of dental implants. A common and time-testedmethod to evaluate biological responses to an implant isto measure the extent of bone implant contact (BIC),referred to as histomorphometry at the light microscopiclevel. Bone implant contact (BIC) is one of the parameterswhich has been used extensively to study the amount ofbone apposition next to the implants [21–27]. When animplant is placed in the jaw, it is in contact with compactbone as well as cancellous bone. The different structuresof the two types of bone frequently result in variation ofmineralized bone-to-implant contact length along theimplant surface [28, 29]. Albrektsson et al. identified thekey features affecting osseointegration about 4 decadesago, e.g., implant surface and topography, surface chemis-try, charge, and wettability [30]. Roughness and enhancedsurface area seems to be helpful for osseointegration.Carlsson et al. reported that screw-shaped implants with arough surface had a stronger bonding than implants witha polished surface [31]. A coarse surface seems to be moreappropriate for osseointegration of implants than a rela-tively smoother implant surface by representing a greaterdegree of implant integration [32–34]. The bone contactareas of 3M™ESPE™ MDIs are surface treated. The treat-ment process of these MDIs includes sandblasting withaluminum oxide particles followed by cleaning and passiv-ation with an oxidizing acid [35].

Despite the advantages of the mini dental implants,evidence on their efficacy and long-term success is lack-ing. The success of these implants will depend on theirunion with the surrounding bone. New implant systemsentering into the market have to be studied with thehelp of animal models first, to demonstrate the osseoin-tegration potential for their probable success in humans.There is a limited evidence regarding the 3M™ESPE™

MDIs. Therefore, there is a need for an animal study toexplore the osseointegration of these implants to assistin better understanding of the treatment selection, prog-nosis, and outcomes for the patients.

Objectives of the studyThe objective of this study is to compare bone appos-ition on the surface of mini dental implants and stand-ard implants by means of histomorphometric methods.

MethodsAnimal modelNine clinically healthy New Zealand white rabbits weigh-ing 3.5 kg and more were used for the study, and theanimals were housed in the central animal house facility.The head of tibia/femur of the animals were usedfor the implantation of samples. Rabbits’ tibiae andfemur have been widely used as an animal model byvarious other authors to study osseointegration ofdental implants [36–45].

Sample sizeThe sample size of this study has been calculated basedon the results of a similar study by Bornstein et al. [22].It was established that 88% statistical power will beachieved by using 18 mini dental implants (3M™ESPE™

MDIs) for the experimental implants and equal numberof an established regular implant (Ankylos®, DentsplyFriadent GmbH) for the control. Therefore, the totalnumber of implants used was 36. Each animal receivedfour implants on hind limbs, i.e., right and left tibia/femur head randomly (the heads of tibia and femur havebeen chosen to get the maximum bulk of bone). There-fore, each animal received two experimental and tworegular implants.

Surgical procedureThe procedures were approved by the institutional ani-mals’ ethics review board of McGill University, Canada.Animals were anesthetized by an intravenous injectionof ketamine hydrochloride-xylazine mixture at 35–50and 1–3 mg/kg respectively according to a method de-scribed by Green et al. [46]. Acepromazine was injectedsubcutaneously at dosage of 1 mg/kg. Further injectionsof the mixture were given to maintain anesthesia, ifnecessary [46]. Sterile ophthalmic ointment was put in

Dhaliwal et al. International Journal of Implant Dentistry (2017) 3:15 of 9

both eyes to prevent corneal desiccation. Animals wereshaved for twice the size of the expected surgical fieldwith an electric razor. All loose hair and debris from theanimal were removed. The surgical area was cleanedwith gauze and 2% chlorhexidine solution to remove themajority of debris from the surgical site. Antiseptic skinpreparation was done starting at the center of the surgi-cal site and moved to the outside of the prepared area ina circular manner. Three scrubs with 2% chlorhexidinesolution and three alternating rinses with alcohol wereperformed. The animal was draped and fixed withclamps on a sterile, impermeable covering to isolate thedisinfected area. This was performed by the gloved andgowned surgical team under sterile conditions.

Surgical protocol for 3M™ESPE™ MDIsA small longitudinal skin incision just distal to the tibia-femur joint was made. The tibia/femur head was ex-posed subperiosteally and an osteotomy performed withthe delicately placed pilot drill over the entry point andlightly pumped up and down under copius saline irriga-tion just to enter the cortical bone for the MDIs. Thiswas used for initial bone drilling to depth of 0.5 mm.The 3M™ESPE™ MDI (size 1.8 mm × 10 mm) vial wasopened and the body of the implant was firmly graspedwith a sterilized locking pliers. The titanium fingerdriver was attached to the head of the implant. Theimplant was transferred to the site and rotated clockwisewhile exerting downwards pressure. This began the selftapping process and was used until noticeable bonyresistance encountered when it touched the lowercortical plate. The winged thumb wrench was used fordriving the implant deeper into the bone, if necessary.All the animals received one MDI on the head of eachtibia or femur. Therefore, total 18 mini dental implantswere inserted.

Surgical protocol for the Ankylos® implantsEqual number of comparator implants (size 3.5 mm ×8 mm) were inserted in the other tibia/femur head ofthe animals after doing the osteotomy according to themanufacturer’s protocol as follows. After mobilizing themucoperiosteal flap, the 3-mm center punch was usedto register a guide for the twist drill. The twist drill wasused to establish the axial alignment of the implant andto assist in the guidance of the depth drill. The depthdrills were sequentially used to create osteotomy to thesubcrestal axial depth of 0.5 mm. The conical reamerwas used to develop the conical shape of the implantbody and to check the osteotomy depth. A counter-clockwise rotation was used to compress the bone in softbone. The tap or thread cutter was used for dense boneto create the threads in the osteotomy. The threadcutter’s diameter corresponds to the implant diameter.

To engage the implant into the implant placement tool,the square faces on the implant fixture mount werealigned with those on the implant placement tool, thenpushed together. Using the handle (finger wheel), theimplant was pulled out of inner vial and the plasticcollar was discarded. The implant placement assemblywas transferred to the osteotomy and the implant wassecured into the osteotomy site. The implant placementwas started with the handle and finally placed using thehand-ratchet. If excessive force was experienced, theosteotomy was rinsed out and the depth was checked byretapping. To disengage fixture mount from implant, theopen-ended spanner was used to break the retentionforce of the fixture mount retention screw. The knurledtop of the implant placement tool was turned by hand tofully disengage the fixture mount with the implant.Pushing down on the knurled top of the implant place-ment tool disengaged the fixture mount.

SuturingExpected length of the procedure was approximately1 h. Following placement of the implants, the woundwas sutured in layers. The underlying muscle, fascia, anddermal layers were sutured with the help of Vicryl (Poly-glactin 910) suture with 3/8 circle reverse cutting needle.The skin was sutured to a primary closer with the samesuture material.

RadiographPlain X-ray images of all the rabbit tibia were taken aftersuturing to confirm the position of implants and to de-tect any injury/fracture of the bone (Fig. 1).

Post surgical treatmentAfter the surgical procedure, the animals were housedin a cage under the supervision of a veterinary doctoruntil they came out of anesthesia. The rabbit was ob-served every 2 h on the first day of surgery followedby once a day to check the wound for infection. Thewound was protected with povidone iodine ointment.The rabbits were allowed immediate weight bearingas tolerated; therefore, they had no restraints onweight bearing.Animals were shifted and housed together with other

rabbits. The rabbit was given a dose of Cephalexin12 mg/kg 0.5 ml I.V. once intraoperatively and a postop-erative analgesic, i.e., Carprofen 2–4 mg/kg S.C. every 8hourly for 3 days according to McGill SOP. The routinedaily care was as per McGill SOP#524.01.The feeding protocols were followed according to the

university central animal house facility guidelines. Theanimals had a free access to water and feed. The sutureswere removed after 7–10 days, and the wound wascleaned with 0.2% chlorhexidine solution.


EuthanasiaThe animals were euthanized at 6 weeks respectively.An overdose of pentobarbital sodium 1 ml/kg intra-venously, under general anesthesia, was used for thispurpose [47, 48].

Specimen retrievalThe implants along with their surrounding bone wereexcised with a surgical saw right away following theeuthanasia. The excess tissue was dissected and the speci-mens were removed en bloc with a margin of surroundingbone of about 5–10 mm. The specimens were immedi-ately put into the 10% formaldehyde solution.

Sample preparation for embeddingThe specimens were dehydrated in the ascending gradedethanol solution and kept in a pre-filtration solution for3 h at room temperature and then in the filtration solu-tion at 4 °C for 17 h. The specimens were then embed-ded in a light curing resin Technovit 9100 NEW (Kulzer& Co., Wehrheim, Germany) polymerization systembased on methyl methacrylate, specially developed forembedding mineralized tissues for light microscopy. Thepolymerization mixture was produced by mixing thesolution A and B in the proportion of 9 parts A and 1part of solution B directly before use. This was done in abeaker and using a glass rod to stir the mixture. Thesamples were then positioned in the labeled plasticmoulds, completely covered in the polymerization mix-ture, and placed in cooled desiccators and under apartial vacuum at 4 °C for 10 min. The resulting blocks

were placed in a sealed container and left to polymerizebetween −8 and −20 °C. The samples were allowed tostand at 4–8 °C in the refrigerator for at least 1 h beforeallowing it to slowly come to room temperature. Thepolymerization times are dependent on the volumes ofpolymerization mixture used and of the constancy of thetemperature at which polymerization is carried out.

Preparation of histological sectionsThe acrylic block was mounted into the object holder ofthe Leica SP 1600 saw microtome (Fig. 2). The height ofthe object was adjusted until the surface of the object isslightly above the upper edge of the saw blade. The sur-face of the block was trimmed to get a plane surfaceprior to producing slices of a defined thickness. Duringthe sawing process, the water flow was adjusted so thatthe water jet lands on the edge of the saw blade. Thebuilt-in water cooling device prevents overheating of theobject and removes saw dust from the cutting edge andthus prolongs the lift time of the saw blade. The mostfavorable feed rate was determined (Fig. 3). After trim-ming, the first undefined slice was removed from thesaw blade. The desired section thickness was selected,considering the thickness of the saw blade and added tothe desired thickness of final section. The section wasstabilized during the sawing process. To do so, a glasscover slip was glued onto the trimmed surface of thespecimen block using cyanoacrylate glue. These blockswere cut with a low speed saw under water along thelateral surface of the implant [47, 48]. The implant

Fig. 1 Radiograph showing implants in the rabbit tibia

Fig. 2 Leica SP 1600 saw microtome


bearing blocks were cut parallel to the long axis of theimplant, and 30-μm-thick specimens were obtained.The saw blade has a thickness of 280 μm and a feed of

310 μm was selected to obtain the final section thicknessof 30 μm. The knurled screw was used for the setting ofthe section thickness. The prepared section was finallyremoved from the saw blade. The specimens wereprepared for histology by the method as described byDonath and Breuner [49].

Histological evaluationSubsequently, the sections were stained with toluidineblue and basic fuchsin similar to other studies [21, 22, 50].The specimen sections were evaluated at the most centralsaggital section of each implant under an optical micro-scope after staining. The images were photographedwith a high resolution camera and interfaced to a moni-tor and PC, observed under the Leica DM2000 micro-scope, and the images were captured using OlympusDP72 camera and associated software [4, 21, 22]. Boneimplant contact (BIC) was measured using InfinityAnalyze software. Six images of the same implant weretaken and measurements were done. The percentage of

the interface contact length between implant surfaceand bone, i.e., bone implant contact (BIC), was calcu-lated. The percentage of bone tissue in a 200-μm-widezone parallel to the contour of the implant area (adjoin-ing the implant) was measured.

Micro-computed tomography (MicroCT)MicroCT scans of each sample of both types of implantswere obtained with a Skyscan 1172 equipment (Kontich,Belgium) at 6 μm resolution with 800 ms exposure time,70 kV electric voltage, 167 μA current, and a 0.5-mmthickness aluminum filter. The equipment was fittedwith a 1.3-MP camera to capture high resolution 2Dimages that were assembled into 3D reconstructionsusing NRecon software supplied with the instrument.

Statistical methodsMean values and standard deviations were calculated forbone implant contact (BIC). Univariate analysis was donefor all the evaluations. Analysis of variance (ANOVA) wasused to analyze the differences between the two implants.P value <0.05 was considered significant. Statistical ana-lyses were carried out with the help of SPSS statisticalsoftware version 18.

ResultsClinical findingsOn the whole, postoperative wound healing in all therabbits was good. None of them exhibited any signs ofwound infection or exposure. A total of 36 specimenswere retrieved for histological examination.

Histological observationsAll of the implants in both groups showed osseointegra-tion and displayed a good amount of bone contactlength (Figs. 4 and 5). No discernible differences werenoticed between both the groups. The zone of interestwas 200 μm in the peri-implant area of the implants onboth sides. Due to large marrow spaces in the rabbit bone,

Fig. 3 Histological sections being obtained with Leica SP 1600saw microtome

Fig. 4 Histological section of mini dental implant in rabbit tibia stained with methylene blue and basic fuchsin


larger volume of bone contact was mostly observed in thecoronal and apical portions of the implants. The MicroCTpictures showed a three-dimensional deposition of bonein both samples (Fig. 6). It was noted that possibility ofnew bone formation was higher in areas adjacent to oldbone. The sections of implant, which were exposed to themarrow spaces, displayed either no bone deposition orvery thin bone tissue. Newly formed bone was seen withlighter staining. In the surrounding areas of both types ofimplants, bone fragments were noticed around the im-plant. These could correspond to bone fragments duringthe osteotomy procedure. Percentage of BIC ranged from45 to 67% in both the groups. The median value of% BIC was 58.5 and the MDI group (IQR 7) andcontrol group was 57.0 (IQR 5.0) (Tables 1 and 2).The mean differences of % BIC between the groupswere verified through Mann–Whitney nonparametrictest. There was no significant difference between the% bone implant contact (BIC) length of both the im-plants (P value >0.05).

DiscussionThe osseointegration potential of 3M™ESPE™ MDIs hasnot been studied. The MDI is a one-piece implant that

simplifies the restorative phase resulting in a reducedcost for the patient. Titanium-aluminum-vanadium alloy(Ti 6Al-4V-ELI) is used for increased strength. The suc-cess of these implants led to its use in long-term fixedand removable dental prostheses [51]. Conventional im-plant treatment requires adequate bone width and inter-dental space. Augmentation procedures are complex andcan cause postoperative pain and discomfort for thepatient and additional costs.In human models, a 3–6-month period is needed to

obtain osseointegration and animal models would need ashorter time (4–6 weeks) [30, 33]. Rabbit has been usedextensively to examine osseointegration and appears tobe an appropriate model for studying the bone healingsystems [52]. The healing periods used by various au-thors for assessing the bone implant contact in rabbitsare 2, 3, 4, 6, 8, and 12 weeks [53–57]. However, the bestresults have been between 6 and 12 weeks of insertionperiod [51, 53–55]. The 6-week healing period was care-fully chosen after literature search. This was in agree-ment with others who have reported that a 6-weekperiod is adequate in rabbits to develop a “rigid osseousinterface” [51–60].At the bone implant interface, woven bone starts

forming after the placement of implant. Lamellar boneslowly replaces this scantily organized bone. The fullydeveloped lamellar bone which replaces the woven bonetypifies a stable and lasting osseointegration [61].Our results are in concurrence with Balkin et al. [62];

they have also shown in their histology study in humansthat the MDI undergoes osseointegration. They insertedone 3M™ESPE™ MDI of 1.8-mm diameter in each of twopatients as a transitional implant for mandibular den-tures. After a period of 4 and 5 months, the implantswere trephined out for histological evaluation. Theresults showed that there was a close apposition of boneon the implant surfaces. The bone surrounding theimplant demonstrated signs of matured healing and inte-grated for immediate function after 4 to 5 months ofhealing period.

Fig. 5 Histological section of standard implant in rabbit tibia stainedwith methylene blue and basic fuchsin

Fig. 6 Micro CT scan images of the MDIs and Ankylos® embedded in rabbit bone 6 weeks post implantation


Our study is also in concordance with the results of aremoval torque study by Simon et al. [63] in immediatelyloaded “transitional endosseous implants” in humans.The percentage BIC for MDIs was similar to standardimplants.The surface topography also affects the BIC, Wenner-

berg et al. [32] measured and compared removal torquevalues on screw-shaped titanium implants with threesurface types. The results showed that screws sand-blasted with 25-μm particles of titanium and 75-μmparticles of aluminum oxide exhibited a higher removaltorque and interfacial bone contact than the machinedtitanium implants with smoother surface texture.The surface of 3M™ESPE™ MDI is sandblasted with

aluminum oxide and cleaned and passivized with anoxidizing acid (Technical Data Sheet, 3M ESPE) [35].The surface of Ankylos® is sandblasted and acid etched[64]. Various authors have reported that surface rough-ness induces a variety of events in the course of osteoblastdifferentiation, spreading and proliferation, production

of alkaline phosphatase, collagen, proteoglycans, andosteocalcin, and synthesis of cytokines and growthfactors [65–67]. Therefore, leading to bone depositionon the surface of these implants, Yan et al. [68] demon-strated that simple surface treatments can turn thetitanium surface into a bone-bonding one. With theresults of our in vitro study, Marulanda et al. [69] ondiscs of both types of implants demonstrated thatsurface chemistry of 3M™ESPE™ MDI is conducive togrowth of osteoblasts leading to bone apposition.One of the shortcomings of our study may be the use

of rabbit tibia as a model. The tibia of the rabbit isessentially hollow except the upper and lower corticalplates. This may justify lack of bone apposition on thewhole implant in both experimental as well as compara-tor implants. However, it provides a reliable informationfor human application as the human maxillary bone isalso of a softer bone quality [36, 51].

ConclusionsThe results of this study show that MDIs as well asregular implants osseointegrate in rabbits.

FundingThis study was funded by Ministère du Développment économique del'Innovation et ce l'Exportation (MDEIE), Gouvernement du Québec, IndianCouncil of Medical Research (ICMR) and 3M ESPE IRB grant numberA10-M118-9A.

Authors’ contributionsJSD carried out the experiments and drafted the manuscript, RAconceived the study and helped in revising the manuscript, MMcontributed to the histological preparation and data analysis, JSFparticipated in this study’s design and overall coordination. All authorsread and approved the final manuscript.

Competing interestsJagjit Singh Dhaliwal, Rubens F. Albuquerque Jr, Monzur Murshed andJocelyne S. Feine declare that they have no competing interests.

Ethical approvalMcGill University Research Ethics Board, Animal Use Protocol #2012-7221. All study procedures were conducted as per McGill SOPs.All efforts were made to minimize distress in animals throughout theexperiments, as well as to use only the number of animals that wasessential to produce reliable scientific data.

Publisher’s NoteSpringer Nature remains neutral with regard to jurisdictional claims inpublished maps and institutional affiliations.

Author details1Faculty of Dentistry, McGill University, 2001 McGill College Avenue, Suite500, Montreal, Quebec H3A 1G1, Canada. 2Faculty of Dentistry of RibeirãoPreto, University of São Paulo, Ribeirão Preto, SP, Brazil. 3Department ofMedicine, McGill University, Montreal, Quebec, Canada.

Received: 22 February 2017 Accepted: 26 April 2017

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Table 1 Comparison of % BIC in both groups

Sample 3M™ESPE™ MDIs Ankylos®

1. 67 54

2. 59 67

3. 54 45

4. 51 58

5. 47 57

6. 64 49

7. 50 54

8. 60 56

9. 56 60

10. 61 53

11. 62 59

12. 61 55

13. 59 59

14. 45 51

15. 58 59

16. 54 62

17. 66 62

18. 56 57

Table 2 Descriptive statistics of the experimental andcontrol group

BIC 3M™ ESPE™ MDIs Ankylos® Friadent (Dentsply)

Median 58.5 57

Mean 57 56.5

Interquartile range 8 5.5

First quartile 53.25 53.75

Third quartile 61.25 59.25


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